Enhanced: How Old Is
the Flower and the Fly?
Conrad C. Labandeira
Science 1998; 280: 57-59.
The first book that Charles Darwin wrote after
publication of The Origin of Species (1859) was On the Various Contrivances by Which
British and Foreign Orchids Are Fertilised by Insects, and on the Good Effects of
Intercrossing (1862) [HN1], an intellectual forerunner to modern
work on pollination biology. In this volume, Darwin applied a tradition of careful
observation with principles such as reciprocal adaptation toward understanding
pollination--one of the most pervasive and diverse of mutualisms known in nature. Orchids [HN2], although fascinating in their own right and the premiere group of
plants renowned for their intimate and intricate coevolutionary associations with
pollinating insects (1) [HN3], nevertheless
represent a relatively recent (Cenozoic) event in the geologic history [HN4]
of pollination. Recently, Friis (2) and others have produced
anatomical evidence from spectacularly preserved floral structures and have elucidated the
first occurrences of pollinator-associated floral features during the mid-Cretaceous.
These angiosperm-[HN5]centered discoveries have pinpointed some of
the earliest known fossil occurrences of particular pollination syndromes. [Pollination
syndromes are morphologically convergent adaptive trends exhibited by both the floral
features of pollinated plants and the mouthpart structure [HN6] and
other flower-interactive features of their respective pollinators (1).]
Nevertheless, the earlier Mesozoic history of insect pollination is considerably more
ambiguous. At present, there are few clues regarding the pollination biology of
"preangiospermous" Mesozoic insects. Most inferences come from modern
associations between primitive lineages of insects and their gymnospermous [HN7] seed plant hosts, especially cycads (3), and
from fossil gut contents and coprolites of pollen-consuming insects (4).
Diagnostic mouthpart structures (4, 5) are rarely
observed, which is now remedied by the discoveries reported by Ren on page 85 of this issue (6). This impressive documentation now places three lineages of lower
brachyceran flies [HN8] [see figure, panel (B)] as
pollinators in China during the Upper Jurassic. However, as explored below, the group of
plants that these external fluid feeders were pollinating is as intriguing as the presence
of the pollination itself.
Pollen consumption (pollinivory) has generally been the evolutionary
precursor to pollination [HN9]. Pollinivory can become a mutualism
(that is, pollination) if the pollinivore can deliver unconsumed pollen to the female
reproductive organs of its host plant more efficiently than alternative dispersal by wind,
splashing rain, or gravity. Pollination mutualisms require a plant to sacrifice pollen for
improved access and efficiency in the fertilization of conspecific ovules. Even
pollinivory is a derived feeding strategy, because it is temporally preceded by spore
consumption (sporivory) in the fossil record. The earliest terrestrial sporivory occurs in
Late Silurian to Early Devonian terrestrial ecosystems, indicated by distinctive
coprolites, produced probably by myriapods [HN10] or insects, with
abundant to occasional spore contents from primitive land plants (7)
[see assemblage 1 in panel (A) of the figure]. During the Carboniferous,
a younger assemblage has been documented [assemblage 2 in panel (A) of
figure], represented by insects. By the end of the period, pollen consumption was
established, evidenced both by well-preserved, dispersed coprolites [panels (D)
and (E) of figure] and gut contents of hemipteroid and orthopteroid
insects (8) [HN11] [panels (F)
and (G) of figure]. Coeval pollination mutualisms have been inferred from
the reproductive biology of certain seed ferns, such as anomalously large pollen grains,
investitures of secretory glands adjacent to reproductive structures, and the presence of
pollination drop mechanisms for attracting pollen and potentially insects (4).
Curiously, elongate mouthparts are known from the Permian (4, 8, 9), probably representing feeding on surface
fluids. The lineages displaying these mutualisms undoubtedly were extinguished during the
late Permian; substantial evidence for pollinivory and pollination does not reappear until
Evolving together. The fossil history of associations between insects and
reproductive structures of vascular plants. (A) The four distinctive
assemblages of fossils (see text for description) representing consumption of spores,
pollen, or nectar, based on a variety of evidence, such as the examples at right. The
presence and intensity of background shading indicate the probable duration and
pervasiveness of pollination. Dots in Late Jurassic denote suites of insects (5, 6) that could be assigned to either assemblages 3
or 4 or both. (B) (Top) Cladogram of major subgroups of the lower
Brachycera [after (16)], showing three fly lineages inferred by Ren (6) to have been Late Jurassic angiosperm pollinators. (Bottom) The head
and proboscis of an extant Australian member of the Tabanomorpha (17).
(C) Ellipsoidal spore-bearing coprolites from Late Silurian (left) and
Early Devonian (right) floras (7). The left specimen consists of plant
cuticle with occasional spores; the right specimen comprises mostly spores. (D)
Late Carboniferous insect coprolite from the Illinois Basin, USA, consisting of pollen
from a cordaitalean gymnosperm, enlarged in (E). (F) A
Lower Permian hypeperlid insect from Russia, with rectal contents illustrated in (G),
containing pollen grains from glossopterid and conifer gymnosperms (8).
(H) The snout weevil Rhopalotria mollis, pollinivore and
pollinator of the extant cycad Zamia furfuracea (3).
F. Marsh/Smithsonian Institution; (C) Nature
377, 329 (1995); (F, G) Lethaia 29, 369 (1997);
(H) Organization for Tropical Studies
Three diverse lines of evidence currently indicate that basal
lineages of modern insect pollinators originated during the Jurassic, probably as
generalists on seed plants [assemblage 3 in panel (A) of figure] (4, 8). First, although recently viewed as exclusively
wind-pollinated, modern cycads [HN12] are now considered
overwhelmingly insect-pollinated (3). Studies now demonstrate beetle
pollinivory in 7 of the 10 extant genera of modern cycads, and apparently faithful
pollination occurs in those species that have been extensively investigated. These
cycad-inhabiting beetle lineages are extant representatives of basal lineages of the
Curculionoidea (weevils and relatives) that originated during the Late Jurassic (10). This shift in received wisdom has also been demonstrated for a
second clade of advanced seed plants, the Ephedrales, of which Gnetum and Ephedra
[HN13] are now known to be insect-pollinated as well, especially by
moths (11, 12). A second line of evidence is
fossil evidence for plant damage, including fecal pellets in chambers evacuated within
bennettitalean strobili [HN14], and coniferalean and ephedralean
pollen in the gut contents of orthopteran and holometabolous insects (4,
8) [HN15]. Last, there has been limited evidence
for pollen- and nectar-imbibing insect mouthparts that are difficult to explain otherwise.
Examples include nemonychid weevils, glossatan moths, and nemestrinid flies (5) [HN16]. To this Jurassic list, Ren (6) adds evidence of elongate mouthparts and body hair patterns from
tabanid, protapiocerid, and additional nemestrinid flies [HN17].
Although Ren indicates that these findings provide evidence for Late Jurassic angiosperms
[initiating assemblage 4 in panel (A) of figure], it is equally likely
that basal brachyceran lineages of flies were pollinating anthophytes other than
angiosperms, lured by exposed sugary fluids secreted by nectaries located on vegetative or
reproductive structures, pollination drop exudates, or even secondarily produced
substances such as honeydew from sap-sucking insects (4, 12, 13). Seed plant candidates include ephedraleans
and cycads and extinct clades such as bennettitaleans, corystosperms, and caytonialeans (1) [HN18].
Ren's (6) documentation of elongated mouthparts
and other pollinator-associated features of Late Jurassic brachyceran flies, bolstered by
recent advances in cycad-weevil pollination biology and the record of mid-Mesozoic
plant-insect interactions, supports the above hypothesis that the origin of modern
lineages of pollinating insects resides amid Jurassic gymnospermous seed plants. If we
accept literally the earliest convincing record of angiosperms [HN19],
well into the Early Cretaceous (11), then those lineages of
pollinating insects that existed during the later Jurassic may have had their mutualisms
subsequently co-opted and fine-tuned by angiosperms. The earliest evidence for fly
pollination in angiosperms is during the mid-Cretaceous, among several early lineages of
angiosperms bearing small, exposed flowers with relatively accessible floral rewards;
however, their floral morphology indicates that their pollinators possessed short,
sponging (labellate) mouthparts (1, 14) and that
they were well established within assemblage 4 [panel (A) of figure].
Deeper throated flowers that require elongate, probing proboscides are relatively derived
in angiosperms (15) and appeared later during the Cretaceous (2). One instructive counterexample to the above pattern of angiosperm
co-optation is beetle pollinators and their cycad hosts, which represent an independent
and parallel development that has persisted to the present (10).
Consequently, investigations of the origins of basal groups of modern pollinating insects
must explore more completely assemblage 3 [panel (A) of figure], of which
there is tantalizing but still incomplete evidence. These investigations will require
extensive examination of Middle Jurassic to earliest Cretaceous compression deposits.
Although there has been considerable effort toward characterizing the insect constituents
of Cretaceous amber, the oldest insect-bearing amber is about 125 million years old and
thus too recent to address the origin of the basal clades of modern insect pollinators.
References and Notes
- M. Proctor, P. Yeo, A. Lack, The Natural
History of Pollination (Timber, Portland, OR, 1996).
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320, 163 (1986) [GEOREF];
W. L. Crepet, Rev. Palaeobot. Palynol. 90, 339 (1996) [GEOREF].
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18, 300 (1986); A. P. Vovides, N. Ogata, V. Sosa, E. Peña-García, Bot.
J. Linn. Soc. 125, 201 (1997).
- C. C. Labandeira, Annu. Rev. Ecol. Syst. 28,
- B. B. Rohdendorf, Ed., Jurassic Insects of
Karatau (Izdatelstvo "Nauka," Moscow, 1968) (in Russian); L. V. Arnol'di,
V. V. Zherikhin, L. M. Nikritin, A. G. Ponomarenko, Eds., Trans. Paleontol. Inst.
161, 1 (1977) (in Russian) [GEOREF];
M. V. Kozlov, Paleont. Zhur. 1989 (no. 4), 37 (1989) (in
- D. Ren, Science 280, 85 (1998).
- D. Edwards, P. A. Selden, J. B. Richardson, L.
Axe, Nature 377, 329 (1995) [GEOREF].
- V. A. Krassilov and A. P. Rasnitsyn, Lethaia
29, 369 (1997).
- V. G. Novokshonov, Paleontol. Zhur. 1997
(no. 1), 65 (1997) (in Russian).
- R. A. Crowson, in Advances in Coleopterology,
M. Zunino, X. BellÇs, M. Blas, Eds. (European Association of Coleopterology, Barcelona,
Spain, 1991), pp. 13-28; R. S. Anderson, Mem. Entomol.Soc. Wash. 14,
- P. R. Crane, E. M. Friis, K. R. Pedersen, Nature
374, 27 (1995) [GEOREF].
- A. D. J. Meeuse, A. H. DeMeijer, O. W. P. Mohr,
S. M. Wellinga, Isr. J. Bot. 39, 113 (1990); M. Kato and T.
Inoue, Nature 368, 195 (1994).
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Entomol. 16, 847 (1987).
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Scand. 24, 407 (1994).
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- I thank P. R. Crane, W. A. DiMichele, B. D.
Farrell, F. C. Thompson, B. M. Wiegmann, and D. K. Yeates for their comments. This is
contribution 39 of the Evolution of Terrestrial Ecosystems consortium at the National
Museum of Natural History.
The author [HN20] is in the Department
of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington,
DC 20560, USA; and the Department of Entomology, University of Maryland, College Park, MD
20742, USA. E-mail: email@example.com
Related Resources on the World Wide Web
- The University of
California Museum of Paleontology (UCMP) at Berkeley presents extensive Web exhibits
about the phylogeny of
living and fossil organisms, geology
and geologic time, and evolutionary
theory; the UCMP Subway
offers links to other Internet resources.
- A collection of links to evolution information on the
Web is maintained by the Biological Laboratories of Harvard University for the World Wide Web Virtual Library. The PaleoNet Pages are maintained by N.
MacLeod. PaleoNet is a system of listservers, Web pages, and ftp sites designed to enhance
electronic communication among paleontologists. There is a mirror site at the Natural History Museum in
- D. Rand, Department of Biology of Brown University (Providence, RI)
provides lecture notes for a course on evolutionary biology that
includes a discussion of coevolution.
- D. Bogler, Division of Biological Sciences, University of Texas at
Austin, maintains a Web site with extensive lecture notes and
Internet links for a course on ecology and evolutionary biology.
- K.-P. Kelber, Mineralogisches Institut, Universitä Würzburg,
Germany, maintains a Web page with annotated Internet links for paleobotanists.
- The Tree
of Life is a project under the direction of D. Maddison, University of Arizona, that
contains information about the phylogenetic relationships and characteristics of all
organisms and provides a map with links to other biological information on the Internet.
- The text of The Origin of Species is
available from the Online Literature Library. J.
Wilkins at the The Walter and Eliza Hall Institute of Medical Research, Victoria,
Australia, maintains a Web page with links to evolution and
Darwin-related Internet resources. The University of South Carolina Library Department of Rare Books
and Special Collections describes Darwin's book on
orchids and insects that it has in its C. Warren Irvin Jr. Collection of Darwin and
- Orchids and related plants are discussed in the
presentation on Orchidales
from the UCMP. The Department of Botany, University of Hawaii, provides an introduction to
the Orchidaceae that
includes a collection of photographs. A collection of orchid images is available from the
Vascular Plant Image Gallery
provided by the Texas A&M University Bioinformatics Working Group. Texas A&M
University's Flowering Plant Gateway
to scientific and other Web resources about the family Orchidaceae.
- The Program in Plant Biology, University of
Maryland, College Park, presents lecture notes on
pollination and pollinators from a course
on general botany. The Insects on
WWW page has collected links to Web sites with information about insects and pollination. M.
McIntosh, Department of Entomology, University of Arizona, provides lecture notes on
pollen use in bees and other insects from a course on insect diversity.
A page about flower
flies is available on the Diptera
Web site from the Systematic Entomology Laboratory of the U.S. Department of Agriculture.
S. Buchmann of the Forgotten
Pollinators Campaign, Arizona-Sonora
Desert Museum, Tucson, AZ, presents a pollination lesson for children.
- The Department of Geology and Geophysics,
University of Alaska Fairbanks, displays a Geologic Time Scale. The
UCMP presents a discussion of geologic
time that includes a hyperlinked geologic time scale.
- The Garden
Web Glossary of Botanical Terms defines angiosperm.
R. Volkwyn, Botany Department, University of the Western Cape, South Africa, discusses angiosperm anatomy. The
Department of Plant Biology, University of Maryland, offers lecture notes on angiosperms from a course
on general botany. A review article titled
"Present state of Angiospermae phylogeny" by R. Spichiger and V. Savolainen is
available from the Web
site of the Conservatoire et Jardin Botaniques de la Ville de Genève, Switzerland.
- The mouthparts of an insect are
illustrated and described in the insect anatomy section of Gordon's Entomological Home Page. J.
Pinto, Entomology Department, University of California, Riverside, offers lecture notes on
mouthpart diversity in insects.
- The Garden
Web Glossary of Botanical Terms defines gymnosperm.
M. Knee, Department of Horticulture and Crop Science, Ohio State University, Columbus,
offers lecture notes
about gymnosperms from a course on general plant biology. J. Reveal, Norton-Brown
Herbarium, University of Maryland, provides a section about gymnosperms that includes
extensive Web links in his lecture
notes for a course in plant taxonomy.
- The Tree of Life Web site's entry for Diptera
describes the suborder Brachycera.
- R. Koning, Biology Department, Eastern
Connecticut State University, Willimantic, provides lecture notes
from a course on plants and human affairs that includes a section on pollination
adaptations. "The yucca plant and the yucca moth" by M. Ramsay and J. R.
Schrock is an article
from the The Kansas School Naturalist about coevolution of those two species
available on the Web from Emporia State University, Emporia, KS. An article
titled "Pollination Biology of Lapeirousia subgenus Lapeirousia
(Iridaceae) in southern Africa; floral divergence and adaptation for long-tongued
fly-pollination" by P. Goldblatt, J. Manning, and P. Bernhardt, is available on the
Web site of the Missouri Botanical Garden,
St. Louis. An article titled
"Prosoeca peringueyi (Diptera: Nemestrinidae) pollination guild in southern
Africa: long-tongued flies and their tubular flowers" by J. Manning and P. Goldblatt
is also available at the Missouri Botanical Garden Web site.
- Coprolite is defined
in the 1913 Webster's Hypertext Dictionary. The Hypertext Webster Gateway has
two entries for myriapod.
The UCMP provides an introduction to the Myriapoda. Here
is a photograph of a fossil myriapod
from the Illinois State Museum's Mazon Creek fossil collection.
- The Neoptera
entry in the Tree of Life Web site discusses the hemipteroid assemblage of insects and the
orthopteroid orders. A table of winged insects that lists the orthopteroid
and hemipteroid orders is provided by A. R. Palmer, Department of Biological Science,
University of Alberta, Canada. The Hemiptera
and Orthoptera are described in
the insect orders section of Gordon's Entomological Home Page. A classification of
Insecta is available from the Kingdoms
Project of the Illinois State Academy of Science.
- A description and photographs of Cycadaceae are available on
the Vascular Plant
Family Access Page maintained by G. Carr, Department of Botany, University of Hawaii
at Manoa. The Garden Web Glossary of Botanical Terms defines a cycad.
The UCMP presents an introduction to the cycads. The Cycad Society is dedicated to the
conservation of cycads through education and scientific research; its Web site includes a photo gallery.
- Photographs of Ephedra and Gnetums are available on the
Vascular Plant Family
Access Page from the University of Hawaii Botany Department. The Hypertext Webster
Gateway provides definitions of Ephedra
Entries for Ephreda
are included in the Classification
of Plants Web site from Manhattan College, Bronx, NY.
- The Garden Web Glossary of Botanical Terms
is defined in the WordNet
database accessed from the Hypertext
- A section on the insect order Orthoptera is
available from the Tree of Life
Web project. J. Meyer, Department of Entomology, North Carolina State University, Ralaigh
provides a page about Orthoptera
in the Compendium
of Hexapod Classes and Orders. The online Merriam-Webster
dictionary defines holometabolous.
J. Pinto, Department of Entomology, University of California, Riverside, defines and
in the lecture notes on insect
metamorphosis for a course on insect morphology.
- The BIOSIS
Web site provides the taxonomic hierarchy used in the Zoological Record for Lepidoptera, which lists
the members of the suborder Glossata. The Nemonychidae is one of the families of Curculionoidea
represented in the Coleoptera collection at the California Academy of Sciences Department of
Entomology. Here is the UCMP page about Coleoptera,
which includes the weevils.
- The family Tabanidae
is described on the Fossil Diptera
Web site maintained by N. Evenhuis, Department of Natural Sciences, Bishop Museum,
Honolulu. N. Evenhuis also provides the Australasian/Oceanian
Diptera Catalog that includes a section about the Nemestrinidae
families of brachyceran flies. Photos of Tabinid flies are
available from the Diptera Home Page of the Systematic Entomology Laboratory, U.S.
Department of Agriculture. Gordon's Entomological Home Page includes a page devoted to the
Tabanidae and other
- On the UCMP Web site Bennettitalales,
Corystospermales, and Caytoniales are grouped under the gymnosperms as
R. Taggart, Department of Botany and Department of Geological Sciences, Michigan State
University, East Lansing, describes and illustrates the difference between Bennettitales (also called cycadeoids)
and cycads. An entry for Bennettitophyta
is included in the fossil plants division of the Classification
of Plants Web site based on Whittaker's Five Kingdom System from the Department of
Biology, Manhattan College.
- K. Willis, Department of Plant Sciences,
University of Cambridge, UK, offers a lecture on angiosperm origins
from a course on the paleobiology
and evolution of plants. The UCMP discusses the origin of Anthophyta
(angiosperms) and the uncertainties and debates surrounding the topic. The UCMP site
includes a chart of the
first appearances of major groups of plants in the fossil record.
- The author is at Department of Paleobiology,
National Museum of Natural History, Smithsonian Institution, and the Department
of Entomology, University of Maryland, College Park.